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Pelagic Polychaetes Rosanna Guglielmo1, Alessandro Bergamasco2*, Roberta Minutoli3, Francesco P

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Pelagic Polychaetes Rosanna Guglielmo1, Alessandro Bergamasco2*, Roberta Minutoli3, Francesco P www.nature.com/scientificreports OPEN The Otranto Channel (South Adriatic Sea), a hot-spot area of plankton biodiversity: pelagic polychaetes Rosanna Guglielmo1, Alessandro Bergamasco2*, Roberta Minutoli3, Francesco P. Patti1, Genuario Belmonte4, Nunziacarla Spanò5, Giacomo Zagami3, Vincenzo Bonanzinga 3, Letterio Guglielmo1 & Antonia Granata3 Composition, density and specimen sizes of pelagic polychaete assemblages were analyzed in the Southern Adriatic Sea. The study was based on fnely stratifed vertical (0–1100 m) and spatial sampling (17 stations) representing spring conditions. Holoplanktonic polychaetes were distributed in both neritic and pelagic waters, although the highest densities were observed along the Otranto Channel. Analysis of the size frequency distribution revealed a trend with depth only for some species. Spatial distribution of holoplanktonic polychaete density was not related to bottom depth, being the organisms mainly concentrated in the epipelagic layer (0–100 m). The most abundant species showed maximum values below or within the thermocline and within the Deep Chlorophyll Maximum or just above it. Relations between polychaete presence and the underlying oceanographic mechanisms regulating the circulation in the Otranto Channel were discussed. The presence of several non- determined polychaete larvae (e.g. Syllidae) in the pelagic waters at 800–1100 m depths suggests the importance of the role of Levantine waters as main actual and potential carrier of species in the area, though a relevant contribution comes also from North Adriatic dense waters through deep spilling and cascading in the Southern Adriatic pit. These fndings increase the knowledge on holoplanktonic polychaetes ecology within the South Adriatic Sea, and represent signifcant data in the monitoring of changes in biodiversity. Polychaetes are a large and diversifed group, widely distributed in freshwater and marine habitats, from the intertidal zone to the deepest sediments. Tere are about 9000 nominal polychaete species in the world1, but their diversity is supposed to be much larger and there are many species that have yet to be described. Most of them inhabit the benthic environment, although several species and a few families have evolved to colonize the pelagic realm, showing hyaline body and large appendages for foating and swimming2–4. Holoplanktonic polychaetes are common in marine zooplankton3, although they are not highly important in terms of abundance5. Some species may, at times, be the dominant forms in the plankton community6–8. Tey are widely distributed in the oceans, mainly in the open sea, but they also occur in neritic region3. Pelagic polychaetes inhabit the entire water column, most species are found in the 100 m thick surface layer9, even if several forms have bathypelagic habits10. In spite of their low abundance in the plankton, but in consideration of a wide range of feeding strategies, holoplanktonic polychaetes play an important role in the pelagic food web11,12 and in organic matter minerali- zation13. Teir trophic ecology is complex: (i) most species are active predators and use their quickly eversible proboscis to attack other zooplankters, such as fsh larvae, siphonophores, chaetognaths and appendicularians 1SZN- Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Napoli, Italy. 2CNR-ISMAR (Institute of Marine Sciences, National Research Council), Arsenale - Tesa 104, Castello 2737/F, 30122, Venice, Italy. 3Dipartimento di Scienze Biologiche, Chimiche, Farmaceutiche ed Ambientali, Università di Messina, 98100, Messina, Italy. 4CoNISMA O.U. Lecce, DiSTeBA-University of Salento, 73100, Lecce, Italy. 5Dipartimento di Scienze biomediche, odontoiatriche e delle immagini morfologiche e funzionali, Università di Messina, 98100, Messina, Italy. *email: [email protected] SCIENTIFIC REPORTS | (2019) 9:19490 | https://doi.org/10.1038/s41598-019-55946-6 1 www.nature.com/scientificreports/ www.nature.com/scientificreports (ii) some others are flter-feeders or phytophagous and (iii) only few species are detritivorous13. In turn, they are a basic food, rich in calories, of numerous fshes3 and of predatory large copepods7. Most studies on holoplanktonic polychaetes have emphasized taxonomy, but ecological aspects are poorly known12. Spatial distribution of the families Typhloscolecidae and Tomopteridae in the tropical eastern part of the Pacifc Ocean is available14,15 as a frst step towards understanding the pelagic polychaete fauna in the tropi- cal western Atlantic region16. Many authors have demonstrated a strong correlation between the distribution of planktonic polychaetes and water masses circulation in the South Atlantic and North Pacifc17–19, or suggested that the structure of holoplanktonic polychaete assemblage (oceanic and neritic) could be determined by the feeding habits of the species and their tolerance to the variability in environmental conditions12. As regards Mediterranean Sea, pelagic polychaetes have been largely neglected respect to the benthic poly- chaete fauna. Monthly changes in composition and abundance of meroplankton and pelagic polychaetes (6 species) of the Cilician Basin shelf waters were reported20, whereas in the checklist of Anellida Polychaeta of the Eastern Mediterranean Sea regions, 14 species of planktonic polychaetes were included from the coasts of Turkey21. More recently, two species of both Typhoscolecidae (Sagitella kowalewski Wagner, 1872 and Typhloscolex muelleri Busch, 1851) and Iospilidae (Phalacrophorus pictus Greef, 1879 and Iospilus phalachroides Viguier, 1886), already included in the checklist of polychaetes of the Italian seas22, have been reported for the frst time in superfcial waters (20–50 m depth) along the northwestern coast of Isola d’Elba (Tuscany)23. Te frst list of all pelagic and benthic polychaetes of the Adriatic Sea was compiled in early nineties24 and included 559 species belonging to 53 families. As for the holoplanktonic polychaetes it is based on several con- tributions during the last century25–32. Compared with earlier studies in the Southern Adriatic Sea, many papers presented data on participation of polychaetes in total zooplankton9,33–35 focusing the attention on the temporal variation of the abundances of some species of polychaetes in order to hypothesize faunal changes associated with the changes of pelagic waters circulation in the South Adriatic through the Otranto channel and on pelagic poly- chaete distribution and seasonal dynamics36. More recently, a complete polychaete checklist of the whole Adriatic Sea was compiled37, in which 24 species of holoplanktonic polychaetes were reported. However, information on the vertical distribution of the holoplanktonic polychaetes population in the diferent hydrographically defned sub-basins remains lacking. Tis study aims at describing the composition and abundance patterns of the holoplanktonic polychaete communities in the Southern Adriatic waters, across the Otranto Channel key area and contributes to fll some knowledge gaps thanks to a fnely stratifed spatial samplings up to 1100 m depth. Te general objectives are to shed light on (1) how the pelagic polychaete distribution and size patterns link to environmental conditions and variability such as horizontal gradients and vertical structure of the water column and (2) how the meso-scale oceanographic circulation can modulate the Northern Adriatic and Ionian inputs of species in the Southern Adriatic Basin, through climate-regulated mechanisms. Methods Study area. Te study area includes the Southern Adriatic basin (maximum depth 1200 m), the Otranto Channel (lat 40°N, lon 19°E, 70 km wide) and its interface with the Ionian Sea, a key region for the regulation of the deep overturning cell of the eastern Mediterranean basin38. In particular, the infuence of the Adriatic Deep Water (ADW) outfow through the Otranto Channel triggered by the formation of dense waters in the Adriatic basin during winter intense cooling events has been put in connection with the periodic reversal of the main upper layer circulation in the Ionian Sea and the consequent alternate advection of Atlantic or Levantine waters in the Southern Adriatic basin (the BIoS mechanism)39. Moreover open-ocean deep convection can be responsible during winter for the production of dense water, generating a mixture of the less saline waters from the Adriatic Sea with the more saline and warmer waters originating from the Ionian Sea40. Te role of the Adriatic Sea as the main source of dense water is known to strongly depend upon the atmos- pheric and thermohaline conditions41. In fact, in the early 1990s the Aegean Sea became the main deep-water formation area (the event is known as the Eastern Mediterranean Transient-EMT), with relevant implications for the water mass properties and circulation of the whole levantine basins42,43. Te mechanism seems nowadays re-established and the Adriatic Sea is returning to dominate the eastern deep-water production44. Te surface layer of the Southern Adriatic basin is characterized by the presence of Adriatic Surface Water (ASW), that mainly fows geostrophically along the Italian coast and features a relatively lower salinity due to the freshwater discharges (Po river) and the Ionian Surface Water (ISW), saltier (S > 38.25) and warmer (T > 15 °C) than ASW, that fows into the Adriatic along the eastern side of the Otranto Channel. During winter, the ISW is spread by the dominating south-easternly winds and in spring it occupies
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